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Cold Atmospheric Plasma Manipulation of Proteins in Food Systems
Tolouie, Haniye; Mohammadifar, Mohammad Amin; Ghomi, Hamid; Hashemi, Maryam
Published in:Critical Reviews in Food Science and Nutrition
Link to article, DOI:10.1080/10408398.2017.1335689
Publication date:2018
Document VersionPeer reviewed version
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Citation (APA):Tolouie, H., Mohammadifar, M. A., Ghomi, H., & Hashemi, M. (2018). Cold Atmospheric Plasma Manipulation ofProteins in Food Systems. Critical Reviews in Food Science and Nutrition, 58(15), 2583-2597.https://doi.org/10.1080/10408398.2017.1335689
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Critical Reviews in Food Science and Nutrition
ISSN: 1040-8398 (Print) 1549-7852 (Online) Journal homepage: http://www.tandfonline.com/loi/bfsn20
Cold Atmospheric Plasma Manipulation ofProteins in Food Systems
Haniye Tolouie, Maryam Hashemi , Mohammad Amin Mohammadifar &Hamid Ghomi
To cite this article: Haniye Tolouie, Maryam Hashemi , Mohammad Amin Mohammadifar &Hamid Ghomi (2017): Cold Atmospheric Plasma Manipulation of Proteins in Food Systems, CriticalReviews in Food Science and Nutrition, DOI: 10.1080/10408398.2017.1335689
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Cold Atmospheric Plasma Manipulation of Proteins in Food Systems
Haniye Tolouiea, Maryam Hashemi
b, Mohammad Amin Mohammadifar
c, Hamid Ghomi
d
aDepartment of Food Science and Technology, Shahid Beheshti University of Medical Science,
Tehran, Iran.
bMicrobial Biotechnology Department, Agricultural Biotechnology Research Institute of Iran
(ABRII), AREEO, Agricultural Research, Education and Extension Organization (AREEO),
Karaj, Iran
cResearch Group for Food Production Engineering, National Food Institute, Technical University
of Denmark, SøltoftsPlads, 2800, Kgs. Lyngby, Denmark
dLaser and Plasma Research Institute, Shahid Beheshti University, Evin, 1983963113, Tehran,
Iran
Corresponding author at: Microbial Biotechnology Department, Agricultural Biotechnology
Research Institute of Iran (ABRII), Karaj, AREEO, Iran. PO Box: 31535-1897, Karaj, Iran E-
mail address: hashemim@abrii.ac.ir (M. Hashemi).
Abstract
Plasma processing has been getting a lot of attention in recent applications as a novel, eco-
friendly, and highly efficient approach. Cold plasma has mostly been used to reduce microbial
counts in foodstuff and biological materials, as well as in different levels of packaging,
particularly in cases where there is thermal sensitivity. As it is a very recent application, the
impact of cold plasma treatment has been studied on the protein structures of food and
pharmaceutical systems, as well as in the packaging industry. Proteins, as a food constituent,
play a remarkable role in the techno-functional characteristics of processed foods and/or the
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physico-chemical properties of protein-based films. At the same time, some proteins are
responsible for reduction in quality and nutritional value, and/or causing allergic reactions in the
human body. This study is a review of the influences of different types of plasma on the
conformation and function of proteins with food origin, especially enzymes and allergens, as
well as protein-made packaging films. In enzyme manipulation with plasma, deactivation has
been reported to be either partial or complete. In addition, an activity increase has been observed
in some cases. These variations are caused by the effect of different active species of plasma on
the enzyme structure and its function. The level and type of variations in the functional
properties of food proteins, purified proteins in food, and plasma-treated protein films are
affected by a number of control factors, including treatment power, time, and gas type, as well as
the nature of the substance and the treatment environment.
Keywords
Cold plasma; Protein structure; Functional properties; Enzymes; Physico-chemical properties;
techno-functional properties.
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1. Introduction
Plasma is considered as the fourth fundamental state of matter. It may be categorized as thermal
or non-thermal plasma, depending on its density and electron temperature (Zhu et al., 2011). All
types of plasma---including high, atmospheric, and low-pressure plasmas, have a broad spectrum
of applications in different fields, such as textile (Huang et al., 2013; Malshe et al., 2013),
electronics (He et al., 2013), life sciences (Pröfrock and Prange, 2012), packaging (Guillard et
al., 2010; Pankaj et al., 2014a), dental applications (Hoffmann et al., 2013; Kim et al., 2014),
sterilization (Lerouge et al., 2001; Moisan et al., 2002; Akitsu et al., 2005; Lee et al., 2006; De
Geyter and Morent, 2012; Klämpfl et al., 2012; Kim et al., 2013; Ziuzina et al., 2013; Cui et al.,
2016), plasma medicines (Weltmann et al., 2012; Laroussi, 2014), and food processing (Banu et
al., 2012). Thanks to the special features of low-temperature (cold) atmospheric plasma
technology---including cost-effectiveness, ability to achieve a moderate temperature in the
vacuum-free systems, and flexibility in practice---many studies have recently been conducted on
cold plasma applications (Oh et al., 2011). In different types of plasma, the formation of reactive
species (especially oxygen, and nitrogen reactive species) can advance some chemical reactions,
such as oxidation, cleavage, or polymerization reactions (Afshari and Hosseini, 2013; Schlüter et
al., 2013; Pankaj et al., 2014a). In addition, ultraviolet irradiation is also reported in both the
short and the long wavelength regions (100--380 nm) in the plasma treatment, which can cause
photochemical reactions (Schlüter et al., 2013). Because of such functions due to the presence of
reactive components, its potential applications in bioscience and food processing has increased in
recent years.
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Food proteins are one of the most important ingredients in the human diet due to their nutritional
value and vital components, as they maintain or create the desired qualitative attributes in many
types of foods (Cannon, 1945). In general, proteins have remarkable effects on the
physicochemical profile, rheological behaviour, and textural and sensory properties of foods.
‘Functional properties’ of proteins are classically defined as the ability to form or stabilize gel-
like networks, films, foams, emulsions, and sols (Foegeding and Davis, 2011). The diversity in
protein functionality is associated with their structure, size, configuration, surface characteristics,
and also the extent and nature of their interaction with other food components, such as
polysaccharides and lipids (Haque et al., 2016).
Most enzymes have protein-based structures that act as an accelerator/enhancer in chemical
reactions. Enzyme catalysts are needed to make biochemical reactions possible (Zaks and
Klibanov, 1984). Many enzymes such as protease, Lipase, amylase, and lactase currently have
wide applications and future potential in the food industry. Enzymes play a significant role in
food preservation; for example, egg-white lysozyme is generally accepted as an antimicrobial
enzyme against clostridia spoilage (Hughey and Johnson, 1987; Roller, 1995). Although the
maintenance of the activity of enzyme added to food for preservation can be a critical concern
during processing, there are certain enzymes that can be involved in unwanted reactions,
resulting in the loss of sensory and nutritional quality (Hendrickx et al., 1998). For such
enzymes, it is especially important to prevent or restrict deleterious enzymatic reactions in order
to provide a high-quality product with extended shelf life. The nutritional and functional
attributes and activities in enzymes are closely associated with their amino acid composition and
sequence, as well as their structural formation (Damodaran, 1994).
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The presence of plasma reactive species can affect proteins and protein-based structures, such as
enzymes. A number of recent papers (Takai, et al., 2012; Surowsky et al., 2013 and 2014;
Tammineedi et al., 2013; Bußler et al., 2015; Mirsa et al., 2015; Zhang et al., 2015; Bahrami et
al., 2016; Lee et al., 2016; Mirsa et al., 2016; Segat et al., 2016) have concentrated on the
fundamental reactions between atmospheric-pressure plasma and proteins, particularly enzymes,
in the model of food systems. They discuss the impacts of plasma on the activity and the
structure of endogenous/exogenous enzymes, and on techno-functional properties of proteins. In
this paper, we review some important aspects of cold plasma application for the manipulation of
proteins in food systems as a possible alternative to the thermal treatment processes.
2. Plasma definition, generation, and classification
“Plasma” mainly consists of positive and negative ions, radicals, electrons, and excited or ground
state of atoms, which results from subjecting a gas to an energy source (Conrads and Schmidt,
2000; Ramazzina et al., 2015). Energy is delivered in sequence to the electrons and the heavy
species via collisions, leading to the destruction of chemical species. For instance, a molecule
can become excited to the extent that it becomes dissociated (Moreau et al., 2008). The gases
utilized in plasma can be air or noble gases like helium and argon, or a mixture of different types
of gases in an appropriate ratio. The type of the applied gas plays a significant role in the
formation of ionization products in plasma processing. For instance, the intermediate products of
pure argon can be inert species or active/ionized argon particles. The majority of the species are
made of dried air---including oxygen and nitrogen active species with an inconsequential content
of trace gases (Niemira, 2012). The plasma energy source (such as thermal, nuclear, and
electrical) and the amount of applied energy in the plasma are other determining factors that can
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affect the temperature and density of the resulting electrons. Based on electron temperature and
density, plasma is classified as high-temperature (thermal) and low-temperature plasma (non-
thermal) (Surowsky et al., 2015). The limitations of thermal plasma include the energy
efficiency, the high quenching effect of chemical reactions, and the operating at temperatures
much higher than ambient temperature, which can impact their applicability to food products
(Moreau et al., 2008).
In non-thermal (cold) plasma, the electron temperature (several ten thousand K) is much higher
than the massive gas temperature (below 310 K) (Knorr et al., 2011). From the thermodynamic
standpoint, this high difference in electron temperature and gas temperature is categorized as
non-equilibrium condition (Misra et al., 2017). Non-thermal plasma can be generated by a
variety of discharge sources at different pressure levels. In plasma system, the lower gas pressure
results in a lower voltage needed for ionization. This intrinsic property of plasma raises the need
for generating cold plasma technologies that operate under atmospheric pressure, and therefore
require less power to generate active plasma (Conrads and Schmidt, 2000). Furthermore, cold
plasma can be described by its generation technology, e.g. corona discharge, dielectric barrier
discharge (DBD), atmospheric pressure plasma jets (APPJ), and microwave discharge (Fridman
et al., 2005).
3. The prominent sources of atmospheric cold plasma
In this section, we briefly describe the prominent sources of atmospheric cold plasma (ACP) and
their characteristics:
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3.1. Corona discharge
Corona discharge utilizes a pair of inhomogeneous electrodes equipped with a high-voltage
system for the ionizing of the gas (Li et al., 2004). The corona is a type of localized emission that
can be ignited with a relatively high electric field at atmospheric pressure. Discharge mainly
occurs near the sharp edges or around the wires, where the electric field is large enough
(Fridman et al., 2005). In corona, the total discharge volume is extensively larger than the
volume affected by the corona action (Eliasson and Kogelschatz, 1991). The operating regimes
and the structures of corona discharge in air, nitrogen, helium, and hydrogen-methane mixture
from a point to a plate electrode configuration were studied by Anato et al. (2009). The corona
discharge structure is spatially non-uniform and is affected by the geometry of the set up. From
an industrial point of view, corona discharge receives a great deal of attention because it can be
applied to bulk gases in the atmospheric or higher pressures at a low temperature (Bárdos and
Baránková, 2010). Cold plasma is stable and in steady condition for a long period of time (Misra
et al., 2017).
3.2. Dielectric barrier discharges
DBD was the most favoured cold atmospheric plasma source (Kogelschatz, 2003; Roth et al.,
2005; Brandenburg, 2017). DBDs use a dielectric barrier to cover one or both of the electrodes in
the discharge gap. DBD discharges---also known as silent discharges---are generally achieved at
high voltages (1--100 kV) and frequencies between 0.05 and 500 kHz, to ignite the gas discharge
without the formation of sparks (Bogaerts et al., 2002; Moreau et al., 2008). The desired voltage
is applied to the one electrode side, while the other electrode is grounded. As a result, any free
electron in the gap is accelerated, thus receiving enough energy to form ions. The DBD
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discharge could operate in different flow regimes, including homogenous glow or filamentary
regime (Misra et al., 2017). The electrode configuration for DBD can be concrete, flat, or
flexible. The flexible electrode configuration has been utilized for the encapsulated plasma
treatment of foodstuff (Yong et al., 2015).
3.3. Atmospheric pressure plasma jets (APPJ)
Winter et al. (2015) reviewed APPJ’s new development and updates in APPJ design. APPJ is
widely used discharge type plasma that consists of two electrodes without any dielectric cover
over them. Pressure plasma jets play an increasingly important role in various plasma processing
applications because of their ability to generate plasma that is not spatially bound or confined by
electrodes (Laroussi and Akan, 2007). Ionized plasma gases pass through a nozzle and are then
directed to the substrate. The electrode gap is about a few millimetres, while the exposure
distance between the nozzle and the substrate can be in the centimetre range. These non-thermal
plasma jet sources typically operate at voltages of 100--1000 V (Ehlbeck et al., 2010).
3.4. Microwave discharge
Microwave plasma transfers energy using electromagnetic oscillations at a frequency below that
of the thermal radiation. Microwave plasma is produced in the frequency of 300 MHz--10 GHz
(Bogaerts et al., 2002). Microwave plasma---one of the most suitable plasma sources---can be
used for surface modification due to the low energy in the resultant plasma ions (Hirose et al.,
1982; Stoffels et al., 2002; Kusano, 2009). An optimization study on the production of stable
microplasma in air and argon by the use of 2.45 GHz microwave excitation was conducted by
Gregório et al. (2009). Although high power levels are often needed for plasma generation in
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microwave systems, the waveguide dimensions may limit the size of the plasma reactor (Bárdos
and Baránková, 2010).
4. Effects of plasma on natural amino acids
All proteins are made up of a linear sequence of natural amino acids. The effect of plasma
exposure on amino acids can generally be discussed under three major categories---health
aspects, protein function and structure, and sensory characteristics. Amino acids are necessary
for the growth, survival, and health of the human body, especially nutritionally essential amino
acids that must be supplied by the food sources. For instance, methionine makes a crucial
contribution to the metabolism of cells (Wu et al., 2013). Methionine is considered as a
hydrophobic essential amino acid frequently found in the interior hydrophobic core (Brosnan and
Brosnan, 2006). In some proteins, a fraction of the methionine residue is somewhat surface-
exposed. This renders them very susceptible to oxidation treatment.
The arrangement and quantity of amino acids determine the ultimate protein shape and function.
For example, cysteine residue in proteins---by virtue of its capability to bond with other cysteine
residues---plays a key role in the formation of disulphide bonds that are especially important in
protein folding and stability (Brosnan and Brosnan, 2006). Some researchers claim that free
amino acids participate directly in taste and also are indirectly involved in flavour development,
because they are the precursors of many odorants (Jurado et al., 2007).
In regard to the aforementioned importance of amino acids in food processing and the human
body, in this section, we review past research works and recent findings on the interactions
between amino acids and plasma species.
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4.1. Role of plasma species and functional molecules
In nonthermal plasmas, the modification of proteins is mainly initiated by reactions with reactive
oxygen species (ROS) in combination with the synergistic effect of reactive nitrogen species
(RNS) (Fig. 1). The minor roles of UV photons and positive or negative particles may also play a
part (Perni et al., 2007). ROS---for instance superoxide radicals or hydroxyl radicals---seems to
be the main contributor to the plasma antibacterial activity (Boudam et al., 2006; Gaunt et al.,
2006). These active species can lead to etching, cross-linking of proteins, and oxidative reactions
in protein building blocks, especially in the side chains of amino acid residues.
Previous studies show that ROS such as •OH can lead to significant changes in protein structure
finally cause the cleavage of proteins into peptides. The course of the oxidation process is
determined by the availability of O2 and O2
.-- (superoxide anion radical) or its protonated form
HO2. (Berlett and Stadtman, 1997). These types of reactions can affect the disulphide bonding
state, as previously reported after exposing arginine vasotocin (a peptide model) by microwave
plasma (Motrescu et al., 2011). The oxidation of sulphur amino acids is the dominant alteration
of proteins during the DBD processing (Lackmann et al., 2015). The main pathway in sulphur--
sulphur bond cleavage could be the addition of an oxygen and hydrogen atom (originated
hydroxyl radical or other active species) to the sulphur-containing atoms to form RSH and RSO,
leading to split-off protein parts.
Another possible pathway can be ascribed to the transfer of non-covalently bound RS or amino
acid sequence or peptide pieces into plasma-treated solution, which causes acidified medium and
accelerates the formation of acidic compounds (Takai et al., 2012).
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The influence of a higher level of acidity on bactericidal capability induced by low-frequency
discharge plasma was investigated by Chen et al. (2008) in treating E. coli. Effective inactivation
was achieved in non-buffered purified water, as a result of the reduction of water pH of 7 to a pH
of 3 (Chen et al., 2008). It was suggested that plasma acidification may involve the formation of
nitrous acid (HNO2) and nitric acid (HNO3) from NO via NO2 (Marouf-Khelifa et al., 2006;
Doubla et al., 2008). Bacteria inactivation using gaseous NO in a liquid phase was demonstrated
by Ghaffari et al. (2006).
Another possible mechanism is the acidic H3O+ ion formation as a consequence of the reaction
between water molecules and hydrogen peroxide (H2O2) (Chen and Lee, 2008).
However, according to a previous study (Khan and Elia, 1991), the modification of amino acids
results from the chemical reactions with plasma-active species in the atmospheric-pressure cold
plasma, rather than chemical degradation by acidic pH.
However, previous research works (Rumbach et al., 2013; Tresp et al., 2013) demonstrate that
the higher protein inactivation efficiency could be seen in an aqueous solution rather than in a
dried state. The barrier effect of the protein molecules in the upper layer of dried materials may
limit the transition of plasma-generated photons RS in the sample, while the solution is exposed
to RS homogeneously. Another reason might be the interaction of solution components with
plasma species, which can contribute to the formation of secondary reactive species, which in
turn can cause further protein inactivation.
4.2. The chemical reactivity of amino acids against plasma
The relative reactivity of all 20 natural amino acids in solution was assessed by Takai et al.
(2014) using a competitive plasma treatment experiment (Takai et al., 2014). The results reveal
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that the contents of methionine, cysteine, and aromatic amino acids were selectively reduced
after plasma exposure. The highest reactivity among the amino acids was observed in
methionine, cysteine, tryptophan, phenylalanine, and tyrosine. They observed that methionine
can be rapidly oxidized by plasma treatment. In agreement with previous studies, it was
suggested that the oxidation of methionine residues takes place faster than the over-oxidation of
cysteine residues (Lackmann et al., 2015). Lackmann et al. (2013) investigated the ability of
plasma processing in atmospheric pressure for GapDH (glyceraldehyde 3-phosphate
dehydrogenase) inactivation. They suggest that cysteine is present in the active site oxidase after
plasma exposure (Lackmann et al., 2013). In this case, some cysteine residues oxidase
preferentially over others, indicating that the amino acid status in the protein conformation might
determine the site of action of active plasma species to some extent.
DBD exposure inactivates RNase A by forming methionine sulfoxide. The subsequent over-
oxidation of cysteines follows the dissociation of disulphide linkages (Lackmann et al., 2015).
Irreversible sulphonation of disulphide-bonded cysteine in glutathione was identified by
exposure to ROS (Deutsch et al., 1999). Consistent with a previous report, disulphide bond
formation between the cysteine thiol groups was found to be feasible by the plasma exposure (Ke
et al., 2010; Ke et al., 2013). Takai et al. (2014) suggest that the formation of disulphide bond
and cysteine sulphonation may happen at the same time (Takai et al., 2014). Kuo et al. (2004)
propose that reactive oxygen species, such as atomic oxygen or OH radicals may attack aromatic
amino acids like tryptophan, which are sensitive to oxidation (Kuo et al., 2004).
Takai et al. (2012) report that the intrinsic fluorescence of tryptophan residues in a protein
declined rapidly during plasma treatment (Takai et al., 2012). Breakdown of L-valine solution
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following the treatment with direct dielectric barrier discharges plasma, resulting in the
formation of products such as formic acid, acetone, acetic acid, and pyruvic acid. Comparably, as
indicated by X-ray photoelectron spectroscopy (XPS), the exposure of L-alanine to direct Ar-
plasma leads to the degradation of COOH and CNH2 groups, especially after being subjected to
ions (Huque et al., 2013).
5. The effect of plasma on the structure and function of proteins
Proteins are biological molecules that have a wide range of functionality among all
macromolecules. The physico-chemical characteristics of proteins in food systems demonstrate
unique functional properties such as their ability to form gels, foams, emulsions, and films. Such
diversity in protein functions is due to the uniquely defined structures and conformation. Each
protein has a specific shape that is held together by covalent, ionic, and hydrogen bonds and
other chemical interactions. Here, we describe the recent developments in the cold plasma
application in the manipulation of food proteins.
5.1. Techno-functional properties of proteins
Proteins are natural polymers that are widely known as functional ingredients in food substances.
They are a component of complicated natural foodstuff such as flour, or they can be isolated as
functional ingredients like gelatins. Such molecular characteristics as chain length, branching,
charge, flexibility, and hydrophobicity largely determine the functional properties in food
matrices (McClements, 2006). The functional attributes can include water-holding capacity,
ability to thicken solutions, gel-forming ability and the capability to form and stabilize emulsions
or foams.
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Table 1 provides a summary of the research findings in the area of improvement of the techno-
functional properties of proteins using cold plasma. The unique properties of the dough and the
baking quality of wheat are mainly affected by the structure and quantity of the gluten proteins
(Becker et al., 2012). Bahrami et al. (2016) suggest that plasma treatment changed the protein
molecular weights and their solubility due to oxidative reactions and consequently their water-
binding capacity and their ability to form the gluten network (Bahrami et al., 2016). Treated
wheat flour proteins had larger molecular weight fractions and lower monomers and proteins,
including albumin and globulin fractions, resulting in enhanced dough strength. These results are
confirmed by a previous work by Misra et al. (2015), who reported changes in the modulus of
elasticity, and the viscosity of strong wheat flour. The alteration of rheological properties could
be related to the enhanced disulphide bonds between gluten in subunits after plasma treatment.
The results are highly affected by input voltage and the time of exposure (Misra et al., 2015).
The effect of ACP treatment on the techno-functionality of protein from Pisum sativum was
investigated by Bußler et al. (2015). They observed 113% and 116% increase in the water and
fat-holding capacities of pea flour after exposure to atmospheric cold plasma for up to 10
minutes. The results of fluorescence measurements confirmed the incidence of conformational
alteration, which can be used to describe the observed effects on the techno-functional properties
of ACP-treated pea flour fractions.
In a recent study, the effect of ACP treatment was investigated for whey protein isolate (WPI)
solutions during treatment times ranging from 1 to 60 minutes (Segat et al., 2015). A small but
significant increase in surface hydrophobicity index was observed until 15 minutes of treatment
due to the slight oxidation in WPI after treatment. Oxidation in WPI modified the side-chain of
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amino acid residues, which in turn resulted in an increase in carbonyl content and the surface
hydrophobicity. Moreover, the strong oxidation of sulphur-containing amino acid side chains---
specially cysteine amino acids or the aggregation among proteins---induced the loss of free SH
groups. It was also reported that foaming improved within 15 min of exposure; however,
following this period, it was reduced significantly although the foam stability increased. The
reason could be the protein aggregation, based on the free SH group analysis, the size
distribution test, and the high-performance liquid chromatography results. This kind of
information is significant, as a better understanding of the fundamental interactions can then be
used to design plasma systems with appropriate conditions that will achieve maximum
efficiency. However, the combination of factors such as the plasma source, gas type, applied
voltage, and substrate state plays an important role.
5.2. Physical and mechanical properties of protein based films
Natural products based on biopolymers, like proteins, have received a great deal of attention for
biodegradable eco-friendly packaging in a bid to reduce the use of synthetic polymers
(Ressouany et al., 1998). Proteins are complex molecules that are composed of polymers of 20
natural monomers. Proteins are related to a broad variety of functionality in foodstuff, especially
a high binding potential between molecules (Cuq et al., 1997). In addition, protein films can
improve the nutritional status of foods (Gennadios and Weller, 1990) and offer a high potential
for forming various linkages and bonds at different sites (Bourtoom, 2009). Many reports have
been published on the improved barrier and the mechanical properties of edible protein-based
films by altering the properties of proteins using chemical and enzymatic treatments, in
combination with hydrophobic materials or polymers, or by using a physical method (Bourtoom,
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2009; Zhang and Mittal, 2010; Wihodo and Moraru, 2013). Regarding the interactions between
plasma and proteins, plasma-induced chemical protein modification may have contributed to the
variation in the physical and mechanical characteristics of food proteins, for instance zein,
caseinate, soy protein isolate, and whey protein, which can be used as components of films and
coatings (Table 2).
Pankaj et al. (2014c) reported that the surface roughness and hydrophilicity of the zein film could
increase after plasma exposure. Similar increases have also been observed for sodium caseinate
film (Pankaj et al., 2014b). Improvement in the hydrophilicity of the films can be associated with
surface oxygenation after plasma treatment (Liu et al., 2004; Pankaj et al., 2014c). The increase
in the ratio of oxygen to carbon atoms indicated that new oxygen-containing groups may form on
the film surface (Pankaj et al., 2014b), leading to a change in the hydrophobic character to
become increasingly hydrophilic (Sparavigna, 2008).
Previous studies show that, depending on the gas source of plasma, various functional groups
such as carboxylic acid, amide bonds, and hydroxyl can be introduced to the surface of polymers
(Desmet et al., 2009; Morent et al., 2011), which may eventually be effective in increasing the
flexibility of the polymer. Oh et al. (2016) suggest that elongation and oxygen barrier property of
defatted soybean meal (DSM) film can increase, following plasma treatment for 15 minutes at
400 W. As a result, plasma exposure limited the oxygen availability in the DSM packaging film,
resulting in the retardation of lipid oxidation of smoked salmon during storage at 4 C (Oh et al.,
2016). As discussed earlier, the presence of radicals on the film surface can form cross-linked
polymer networks (Stutz et al., 1990), which results in the reduction of the network free volume
and limits the O2 permeability of the film (Perez‐gago and Krochta, 2001). This presumption was
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further supported by the research findings showing a reduction in O2 barrier property in polymer
by Ar-induced cross-linking (Houston et al., 2002). Other researchers suggest that cold plasma
treatment may alter the solubility, but not the diffusivity, of water molecules, so that the bulk
property of water vapor permeability may remain unchanged (Shriver and Yang, 2011; Oh et al.,
2016). Pankaj et al. (2014) found that the intensity of the amide II band increased after DBD
plasma treatment due to the occurrence of a shift from a β-sheet structure to an α-helical
configuration and the formation of more extensive hydrogen bonding between the proteins,
leading to a reduction in the non-bonded peptide groups in the zein films (Pankaj et al., 2014c).
In contrast, the FTIR spectrum results of the plasma-treated sodium caseinate film showed no
significant changes in the peptide linkages and the helical structure of the protein (Pankaj et al.,
2014b).
Over recent decades, some researchers have investigated the application of encapsulation for
functional food components and drugs in the suitable edible delivery system (Dai et al., 2005;
McClements et al., 2009; deVos et al., 2010; Tavares et al., 2014). A large diversity of food
proteins (for example whey protein, casein, gelatin, wheat gluten, and myosin) is accessible as
building blocks in the formation of delivery systems (McClements et al., 2009). Previous studies
indicate that the biocompatibility and release capability of proteins are closely related to their
molecular properties, including structural properties, conformational characteristics, and thermal
stability (Mitragotri et al., 2014; McClements et al., 2009). As discussed before, some studies
have demonstrated that ACP exposure can selectively alter the protein conformation and
function, depending on biological origin, plasma type, and treatment condition. However, there
is still a lack of investigation on the possible benefits of ACP treatment for improving the
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encapsulation efficiency. Zhu et al. (2016) observed that thermal stability, electrical properties,
and mechanical strength of drug-encapsulated nanoparticles are ameliorated by the impact of
ACP. Hasirci et al. (2010) suggest that plasma exposure can lead to the higher hydrophilicity of
poly D, L-lactide-co-glycolide (PLGA) films and consequently enhanced cell adhesion. The
authors suggest that ACP application can contribute to encapsulation systems by changing the
molecular properties of proteins, subsequently leading to higher encapsulation loading efficiency
and delivery response.
5.3. Enzyme structure and function
Enzymes are biocatalysts that are able to manipulate all the main groups of biomolecules found
in foodstuff. In many cases, enzymatic activity should be considered for product shelf life
extension. Several attempts have been made earlier to improve food shelf life using cold plasma.
The selected relevant researches are listed in Table 3.
Segat et al. (2016) evaluated the effect of dielectric barrier discharge plasma on the alkaline
phosphatase activity of milk (Segat et al., 2016). Following the ACP treatments, regardless of the
voltage applied after 120 seconds of treatment, the enzyme activity decreased by around 45--
50%; after 180 seconds of exposure, the activity was reported to be below 10%. Fridman et al.
(2008) show that plasma affects proteins quite selectively. They also report the influence of
plasma on trypsin activity, where the enzymatic activity of trypsin dropped to about zero after
10--15 seconds of ACP exposure (Fridman et al., 2008). According to Surowsky et al. (2013),
180 seconds of treatment can reduce about 90% of the polyphenoloxidase (PPO) activity,
whereas peroxidase (POD) was not as sensitive as PPO, and the enzymatic activity decreased by
about 85% after 240 seconds of treatment. The PPO activity was reduced significantly following
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the addition of low levels of oxygen to argon compared to its activity while using pure argon.
Tappi et al. (2014) observed up to about 42% linear reduction of the PPO residual activity in
freshly cut apples by increasing the exposure time to 10, 20, and 30 minutes in the applied DBD
system. The inactivation of PPO and POD enzymes in freshly cut apples and potatoes by
microwave plasma during 10 minutes of plasma treatment has been investigated by Bußler et al.
(2016). They report that the activity was reduced by about 62% and 77% in freshly cut apples
and potatoes, respectively.
Zhang et al. (2015) investigated the possibility of the inactivation of lactate dehydrogenase
(LDH) enzyme solutions by the helium-oxygen cold DBD plasma in two types of exposure
(direct and indirect). Regardless of the treatment mode, the LDH activity decreases with the
increase in treatment time. However, compared to the indirect treatment, a faster reduction rate
in LDH activity was observed in the direct exposure for the exact time. This may be due to the
diversities in the reactive species (RS) in both modes. They suggest that in the indirect mode, the
long-lived RSs, such as H2O2, and O3 in the solution, play a major role in the plasma
inactivation. However, in the direct treatment, in addition to the mentioned RS, the short-lived
RSs such as OH˙ and O2 as well as UV may be related to the enzyme inactivation of ACP.
Pankaj et al. (2013) studied the effects of treatment time and voltage of the DBD plasma process
on the activity of tomato peroxidase (Pankaj et al., 2013). They observed that the enzymatic
activity decreased with both treatment time and voltage. The interaction between voltage and
time was also significant. Between these two variables, the influence of voltage on inactivation
rates was more pronounced.
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Although in the majority of research studies, cold plasma leads to inactivation of enzymes, an
increase in enzymatic activity is also reported in some cases. El-Aziz et al. (2014) studied the
effect of the atmospheric pressure plasma jet on Plodiainterpunctella for insect control. They
investigated antioxidant enzymatic activities, catalase glutathione S-transferase, and lipid
peroxidase as markers of the oxidative stress in the body tissues of Indian meal moth larvae.
Treatment with 15 pulses at a distance of 11 cm from the jet nozzle significantly increased the
activity of catalase and lipid peroxide. No change in glutathione peroxidase was observed after
24 hours. Excessive oxidative damage led to an enhanced regulation of antioxidants regarding
the insects’ physiological adaptations and resistance. Li et al. (2011) examined the effect of the
radio-frequency atmospheric-pressure plasma jet on the lipase activity originating from Candida
rugosa (Type VII, L-1754) (Li et al., 2011). In this experiment, in the presence of Helium as the
plasma working gas, the measured enzymatic activity of the lipase enhanced by increasing the
plasma treatment time up to 50 seconds. The treatment did not affect the activity of the lipase in
the lipase-buffer mixture. Chen et al. (2016) reported up to 162% increase in the activity of α-
amylase in brown rice treated by low-pressure plasma at 3kV power input over 24 hours of
germination (Chen et al., 2016). This result is in agreement with the findings of Lee et al. (2016).
Puač et al. (2014) also found that the activity of superoxide dismutase (SOD) and catalase (CAT)
enzymes increased following the exposure of carrot cells to atmospheric radio-frequency plasma.
Therefore, this may be true if the cells were not lethally damaged. The inactivation/activation of
enzymes when they are exposed to plasma mainly depends on the ability of the defence system
to confront stress-induced RS (Puač et al., 2014).
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It is noteworthy that any kind of enzymatic activity variation---regardless of the positive or
negative effects---results from the modification of secondary and tertiary structures and changes
in sensitive amino acids (Li, Wang, 2011). Figure 2 schematically summarizes the key steps for
the enzyme inactivation by cold plasma.
Table 4 shows several findings of changes in the protein structure after exposure to cold plasma.
The study by Deng et al. (2007) reports that exposure of bovine serum albumin to atmospheric-
pressure glow discharge plasma degraded protein integrity (Deng et al., 2007). The possible
suggested mechanisms for enzyme inactivation relied on the works done on egg white lysozyme
as an enzyme model in an aqueous solution, using a low frequency helium plasma jet system, as
suggested by Takai et al. (2012). In their study, mass spectroscopy, circular dichroism, and
fluorescence measurement were used to examine the structural changes of lysozyme. The results
indicate that the low frequency plasma jet modifies some amino acid residues and unfold the
secondary structure of lysozyme. These alterations are mainly caused by the action of reactive
oxygen and nitrogen species, which could oxidize reactive amino acids such as cysteine,
aromatic rings of phenylalanine, tyrosine, and tryptophan and as a sequence change the
secondary and tertiary structures of the enzyme configuration. Segat et al. (2016) investigated the
pattern and extent of changes in the structure of alkaline phosphatase through circular dichroism
studies and chemometric analysis. They found that inactivation could happen due to the loss of
α-helical and β-sheet secondary structures of the protein (Segat et al., 2016). The reason for the
loss of lactate dehydrogenase (LDH) activity was investigated by circular dichroism and
dynamic light scattering (Zhang et al., 2015). There was a sharp decrease in the turns and α--
helix structures with an increase in the treatment time, whereas the percentage of random areas
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and the amount of β-sheet contents increased remarkably, indicating that the secondary structure
of the LDH enzyme was altered by the plasma. This result was in agreement with those reported
by Surowsky et al. (2013) that simultaneous reduction of α-helix structure and increase of β-
sheet content can be attributed to the inactivation of peroxidase and polyphenol oxidase in a
model food system, exposed to cold plasma treatment, which has been confirmed by circular
dichroism and tryptophan fluorescence measurements (Surowsky et al., 2013). The tryptophan
fluorescence measurements were considered as a pointer of oxidation reactions, the following
modification in the three-dimensional structure, and the conformation of proteins.
However, the induced plasma changes on enzymes may be temporary, since the alterations in the
enzyme structure tend to partially recover to an untreated state upon storage. Partial recovery in
the LDH structure, which was treated by 300 seconds of plasma exposure, was reported after 24
hours of storage (Zhang et al., 2015). The reason could be the unique properties of each protein,
which cause different sensitivity to plasma treatment. Such reports underlining the application of
cold plasma in the enzyme field would require careful design to be useful for incorporation in
food processes with a specific purpose. However, information about changes in the treated
enzymes function and structure during the time still remains limited.
6. Food allergenicity
Food allergy has been a rising phenomenon for a long time and is considered a public health
issue, especially in developed countries. A great number of food allergens are proteins or water-
soluble glycoproteins with a molecular weight range 10--70 kDa (Besler, 2001).
Antibodies, namely immunoglobulin E (IgE), are an immunoglobulin subclass produced by the
immune system. They are capable of binding to the allergens at a specific site (epitope), resulting
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in various immunologic reactions. Changes in protein configuration can make changes in
epitopes to the extent that they can no longer be identified by IgE antibodies or give any clue to
immune response (Shriver and Yang, 2011).
Recent studies indicate that cold plasma has a potential for reducing the immunoreactivity of
wheat and shrimp proteins (Nooji, 2011; Shriver, 2011). Meinlschmidt et al. (2016) investigated
the impact of ACP on soy immuno-reactivity to control soy allergy (Meinlschmidt et al., 2016).
Following the cold plasma, a reduction in protein intensity bands corresponding to major soy
allergens (i.e. β-conglycinin (Gly m5) and glycinin (Gly m6)) was observed. Moreover, soy
immunoreactivity was lost by up to nearly 100%. These findings were revealed by SDS-PAGE
analysis and Sandwich ELISA assessment respectively. Shriver (2011) found a remarkable
decrease in the allergenicity of shrimp tropomyos by up to 76% due to air-generated DBD
plasma (30 Kv, 60 Hz, five minutes) (Shriver, 2011). Nooji (2011) also reported reduction in
wheat allergenicity up to 37% after five minutes of applying direct DBD plasma with 30 kV
input power (Nooji, 2011). In contrast to the above studies, Tammineedi et al. (2013) observed
no alteration in the antibody-binding capability of α-casein and whey solution as major milk
protein allergens after exposure to plasma afterglow (Tammineedi et al., 2013). Based on the
report by Besler et al., several processing technologies may change food allergenicity caused by
immunoglobulin E antibody (Besler et al., 2001). However, the influence of ACP on the
proteinaceous inhibitors that exert the negative nutritional effects has not been investigated yet.
7. Challenges and future research prospect
Nowadays, the majority of procedures performed to change the protein activity or functions are
based on thermal processing. However, recently, cold plasma has received a great deal of
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attention as a novel nonthermal approach to modify protein or proteinaceous matters in a desired
manner. Recent studies show a variety of plasma applications in the field of inactivation of
deteriorating enzymes, improvement of physical and mechanical characteristics of films, and
techno-functional characteristics of food components, as well as a reduction in allergenicity
arising from food. There are multiple known mechanisms that can affect protein. However, the
most important reason may be the alteration in protein conformation induced by plasma reactive
species. The cleaved peptide bonds, oxidized amino acid side residuals, and form the protein--
protein cross-linkages. These are examples of changes presumably resulting in the destruction of
the protein structure. Based on our literature reviews, the research on the proposed mechanisms
of interaction of cold plasma species and proteins is limited. There is great potential for further
investigation on the improvement of understanding of these mechanisms in molecular scale and
the development of kinetics of reactions. It should be considered that the chemistry of cold
plasma is complex. For example, plasma in humid air consists of more than 75 species (Misra et
al., 2016). This large number of species will lead to nearly 450 reactions (Kossyi et al., 1992).
The chemistry of plasma can change depending on the gas mixture and the applied voltage.
Utilizing the cold plasma technology in a large scale will require monitoring and controlling the
plasma chemistry. The rheology and thermodynamic of plasma is another important aspect that
require intensive modelling and research works. Misra et al. (2017) make use of Boltzmann
equation for species combined with Navier--Stokes equations for the gas flow to understand the
rheology of cold plasma. These equations include coefficient that can be estimated using
experimental data. Resolving these equations will require computational fluid dynamic (CFD)
tools. The combination of experimental findings and CFD results will help in the great
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understanding of impact of the geometry, gas mixture and voltage on the efficiency of cold
plasma and design of the most efficient system. This research area is very immature and further
investigations are required.
Plasma can destruct microorganisms; therefore, it can be used as a surface cleaning tool for the
removal of disinfections and also for cold sterilization. Despite the extensive research on the
inactivation of microorganisms by cold plasma and their large-scale applications in biomedical
sectors (Soloshenko et al., 2000; Moisan et al., 2001 and 2002), the studies on the inactivation of
enzymes by using cold plasma are still limited to the small or lab-scale. Most of these studies
have been performed under simplified conditions in a buffer environment. These researchers
have demonstrated successful inactivation of enzymes in a short period of time. However, these
results must be validated in real food systems before coming to any conclusion. There are
demands for studies to be performed on the possible changes in the activity of enzyme during the
storage of treated material with cold plasma (Zhang et al., 2015). The storage conditions need to
be set to ensure that the enzyme activity is not recovered. This aspect has been less attended in
the previous research works and requires further investigations. The changes made by plasma to
the formulation of food recipes or conformation of food components could have unforeseen
consequences on the final product quality (Pinela and Ferreira, 2015) and safety, as this would
result in the temporary or permanent removal of some protective effects such as the lowering of
water activity and reduction in antioxidant capacity. Accordingly, there is still a need for more
comprehensive studies on the consequences of plasma protein manipulation in both in vitro and
in vivo conditions to ensure the health of food supplies. It is especially remarkable in food
products that claim to have high nutritional value and healthy properties.
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The cost aspect of cold plasma treatment is still unclear. This cost includes both operating and
capital costs to set up a cold plasma technology for a large-scale treatment process. This is due to
the fact that the success of plasma treatment technology is eventually dependent on its economic
viability. This seems to be a great prospect for future research. It is also very interesting to
compare the cost and effect of plasma treatment with those of thermal treatment as a commonly
used technique.
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Table 1: Results of cold plasma influence on physical and mechanical properties of protein
based films Food component/
property
Matrix Plasma Source Treatment Conditions Results References
Gas type Max time Mode of
exposure
Defatted soybean meal DSM/ glycerol Low pressure
microwave
powered
O2, N2, Air, He,
Ar (1 std L/min)
25 min Direct -Increase in
polymer surface
roughness
(Oh, Roh, 2016)
(DSM) -based film cold Plasma (2.45
GHz, 650 W)
-Increase in ink
adhesion by O2
and air plasma
gas
-Increase in the
film elongation
by using O2, N2,
He, and Ar as
plasma gas
-Increase in film
lightness by
using N2 and Ar
by using plasma
gas.
Zein film Zein/ ethanol/
glycerol
DBD Air (48% RH) 5 min Direct -Increased the
surface
roughness and
equillibrium
moisture content
of the
(Pankaj, Bueno‐Ferrer,
2014c)
(80kV, 50 Hz) Zein film in a
direct
relationship with
the applied
voltage level.
-No significant
difference in the
thermal stability
Sodium caseinate film Glyce rol/
sodium
caseinate
DBD Air 5 min Direct -Increase in the
surface
roughness
(Pankaj, Bueno-Ferrer,
2014b)
(70 kV, 50 Hz) (53% RH) -Increase in the
hydrophilicity
DBD-Dielectric barrier discharge
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Table 2: Recent studies on the influence of plasma treatment on the techno-functional properties
of proteins
Food component/
property
Matrix Plasma Source Treatment Conditions Results References
Gas type Max time Mode of
exposure
α-casein Sodium
phosphate
buffered saline
(pH 7.4)
Plasma jet (13.56
MHz)
Ar (30.7 l/min) 15 min Indirect -No changes in
allergenicity
(Tammineedi,
Choudhary, 2013)
Whey protein (β-
lactoglobulin and α-
lactalbumin)
-No noticeable
change in gel
band intensities
and protein
concentration
(DS-PAGE
results)
-No significant
difference in IgE
binding values
(Ci-ELISA
analysis)
Whey protein
isolate (including β-
lactoglobulin,α-
lactoalbumin, and
bovine serum
albumin)
Phosphate
buffer (pH 6.8)
DBD (70 kV,
discharge gap 44
mm)
Air 60 min Direct -Increase in
yellow colour
(Segat, Misra, 2015)
-Decrease in pH
-Mild oxidation
in the proteins
-Improvement in
foaming and
emulsifying
capacity
Wheat flour - Plasma discharge
by DC power
supply (20 V, 9
kHz)
Air 120s Direct -Stronger dough
(Reomixer)
(Bahrami, Bayliss, 2016)
Hard and soft wheat
flour
- DBD Air (45 ± 1%
relative
humidity)
10 min Direct -Improvement in
the dough
strength and
optimum mixing
time
(Misra, Kaur, 2015)
(50 Hz, 70 kV)
Pea protein
isolates(crude
protein content
81.2%)
Freeze dried
and grinded
pea protein
isolate powder
DBD (8.8 kVPP,
3.0 kHz)
Air 10 min Semi-direct -Increase in
water and fat
binding
(Bußler, Steins, 2015)
-Increase in the
protein solubility
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-Decrease in
solubility during
storage (except
for an exposure
to plasma for 1
min)
- Structural
changes
(Fluorescence
spectra results)
DBD-Dielectric barrier discharge
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Table 3. Recent findings of changes in the enzyme activity following plasma exposure
Food component/
property
Matrix Plasma Source Treatment Conditions Results Reference
Gas type Max time Mode of
exposure
Peroxidase Peroxidase
extract from
tomatoes
DBD (50 kV,
electrode gap 26
mm)
Air (42% relative
humidity)
5 min Direct -Decrease in
activity
(Pankaj, Misra, 2013)
-Sigmoidal
logistic
inactivation
kinetics
-Peroxidase Two-layer
model food
system (base
on gellan gum)
Plasma jet (HF,1.1
MHz, 65 V)
Ar 0.05% (0.01and
0.1% O2)
6 min Direct -Decrease in both
enzymes activity
(Surowsky, Fischer, 2013)
-Polyphenol
oxidase
-Polyphenol
oxidase was
more stable
-0.1% oxygen
was the most
suitable gas
composition
-Superoxide
dismutase
Maize roots
(after treating
seeds)
Diffuse Coplanar Ambient air 2 min Direct In the 3-day-old
roots:
(Henselová et al., 2012)
-Uaiacol-
peroxidase
DBD -A slight,
significant
increase in
superoxide
dismutase
activity
-Catalase (14 kHz) -Decrease in
Catalase activity
-Dehydrogenase -Decrease in
uaiacol-
peroxidase
activity
-Decrease in
Dehydrogenase
activity with the
time of
treatment.
- α-amylase Brown rice Low pressure plasma
system (DC high-
voltage supply, 3
kV)
Air 30 min Direct -Decrease in α-
amylase activity
in early storage
period
(Chen et al., 2015)
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-Lipoxygenase -Decrease in
lipoxygenase
activity in
storage period
-Significant
decrease in
lipoxygenase
activity by
increasing
thevoltageof
plasma
-Catalase Plodiainterpun
ctella
Plasma jet (20 kV,
gap between
electrodes of 2-3
mm)
Air Base on
pulses (1, 5,
10, 15 or 20
pulses)
Direct -Plasma causes
oxidative damage
in P.
interpunctella
larvae
(El-Aziz, Mahmoud, 2014)
-Glutathione S-
transferase
-Increase in
catalase and
glutathione S-
transferase
activities.
-Lipid peroxidase -No significant
changes in lipid
peroxidase
activity
-Increases in
mortality with
increase of
plasma pulses
-Increases in
mortality with
increase of
distance from the
nozzle
Lactate
dehydrogenase
Phosphate
buffer solution
(PBS, pH: 7.5)
DBD (24 kHz,
discharge gap 5 mm)
He-O2 (80 L/h -10
L/h respectively)
1h Direct/ indirect -Decrease in
activity with
exposure time
regardless of
treatment modes
(Zhang, Xu, 2015)
-Less reduction
inenzymatic
activity in the
indirect treatment
for the same time
-Increasein
enzymatic
activity after
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storage
-Recovery trend
after storage (24
h)
Glyceraldehyde 3-
phosphate
dehydrogenase(GA
PDH)
in vitro: Microscale plasma
jet (230 Vr.m.s., 13.56
MHz)
He + 0.6% O2 600 s Direct -Much more
effective
inactivation in
the living cell
than in vitro
conditions
(Lackmann, Schneider, 2013)
(dissolved in 1
mg
ml1
distilled
water and
deride)
-Inactivate
proteins in the
cellular milieu,
physical damage
to the cellular
envelope,
modifications to
DNA and
proteins
contribute to the
bactericidal
properties of
plasma
in vivo:
E. colias a
model
organisms
(in potassium
phosphate
buffer pH:7.4)
DBD-Dielectric barrier discharge
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Table 4. Overview on studies dealing with the effect of cold plasma on protein structure
Food component/
property
Matrix Plasma Source Treatment Conditions Results Reference
Gas type Max time Mode of
exposure
Egg white
lysozyme
Phosphate buffer
(pH 7.4)
low-frequency
plasma jet (13.9
kHz)
He (0.5 l/ min) +
O2
30 min Direct -Mass shift to
high molecular
weight
(Takai, Kitano, 2012)
(0.15 l/ min) -Unfolding
-Change in the
secondary
structure
-Modification of
some amino acid
side chains (E.g.
cysteine,
phenylalanine,
tyrosine, and
tryptophan)
Lactate
dehydrogenase
Phosphate buffer
solution (PBS,
pH: 7.5)
DBD He-O2 (80 L/h-
10 L/h
respectively)
1h Direct/ indirect -Changes in the
secondary
molecular
structure
(Zhang, Xu, 2015)
(24 kHz,
discharge gap 5
mm)
-Polymerization
of the peptide
chains (according
Circular
dichroism and
dynamic light
scattering results)
whey protein
isolate
(including β-
lactoglobulin,α-
lactoalbumin,
and bovine
serum albumin)
phosphate buffer
(pH 6.8)
DBD (70 kV,
discharge gap 44
mm)
Air 60 min Direct -Increase in
carbonyl groups
(Segat, Misra, 2015)
-Increase in
surface
hydrophobicity
-Increase in the
size distribution
and the
polydispersity
index
Wheat flour - plasma discharge
by DC power
supply (20 V, 9
kHz)
Air 120s Direct -No significant
change in the
total protein
levels
(Bahrami, Bayliss, 2016)
-Shift towards
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larger molecular
weight proteins
(SE-HPLC
results)
hard and soft
wheat flour
- DBD Air (45 ± 1%
relative
humidity)
10 min Direct -Change in the
secondary
structure of
proteins:
(Misra, Kaur, 2015)
(70 kV, 50 Hz) -Decrease in β-
sheets
-Increase in α-
helix and β-turns
(FTIR
spectroscopy
result)
Pea protein
isolates (crude
protein content
81.2%)
freeze dried and
grinded pea
protein isolate
powder
DBD (8.8 kVPP,
3.0 kHz)
Air 10 min Semi-direct -Increase in
water and fat
binding
(Bußler, Steins, 2015)
-Increase in the
protein solubility
-Decrease in
solubility during
storage (except
for an exposure
to CAPP for 1
min)
- Structural
changes
(Fluorescence
spectra results)
glyceraldehyde
3-phosphate
dehydrogenase(
GAPDH)
in vitro: Microscale
plasma jet (230
Vr.m.s., 13.56
MHz)
He + 0.6% O2 600 s Direct -No significant
loss or
fragmentation of
GAPDH in vitro
(assessed by
SDS--PAGE)
(Lackmann, Schneider,
2013)
(dissolved in 1
mg ml1
distilled
water and deride)
in vivo:
E. coli as a
model organisms
(in potassium
phosphate buffer
pH:7.4)
DBD-Dielectric barrier discharge
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Fig. 1 Research areas in the manipulation of proteins in food systems with cold atmospheric
plasma
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Fig. 2 Schematic of enzyme inactivation by plasma (ROS: Reactive oxygen species, RNS:
Reactive nitrogen species)